Invited review: Plasticity in the control of breathing following sensory denervation

Journal of Applied Physiology

Volumn 94, Issue 2, 2003, Pages 784-794

  Forster, H V ^a  

^a CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Chemoreflexes; Mechanoreflexes; Receptors; Recovery of function; Redundancy

Indexed keywords

SEROTONIN;

AGE; AORTA CHEMORECEPTOR; BREATHING MUSCLE; CAROTID BODY; CENTRAL NERVOUS SYSTEM DISEASE; CERVICAL SPINAL CORD; CHEMORECEPTOR REFLEX; CONVALESCENCE; DENERVATION; DORSAL RHIZOTOMY; HERING BREUER REFLEX; LUNG RECEPTOR; MECHANORECEPTOR; MOTONEURON; MUSCLE DENERVATION; NERVE CELL PLASTICITY; NONHUMAN; PHRENIC NERVE; PONS; PRIORITY JOURNAL; RESPIRATION CONTROL; REVIEW; SENSORY SYSTEM; UPREGULATION; ANIMAL; BREATHING MECHANICS; CHEMORECEPTOR; HUMAN; NERVOUS SYSTEM FUNCTION; PHYSIOLOGY;

ANIMALS; CHEMORECEPTORS; DENERVATION; HUMANS; MECHANORECEPTORS; NERVOUS SYSTEM PHYSIOLOGY; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; RESPIRATORY MECHANICS;

EID: 0037311622     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00602.2002     Document Type: Review

References (100)

1. Akilesh MR, Kamper M, Li A, and Nattie EE. Effects of unilateral lesions of retrotrapezoid nucleus on breathing in awake rats. J Appl Physiol 82: 469-479, 1997.
2. Banner NR, Lloyd MH, Hamilton RD, Innes JA, Guz A, and Yacoub MH. Cardiopulmonary response to dynamic exercise after heart and combined heart-lung transplantation. Br Heart J 61: 215-223, 1989.
3. Berger AJ and Cooney KA. Ventilatory effects of kainic acid injection in the ventrolateral solitary nucleus. J Appl Physiol 52: 131-140, 1982.
4. 2 breathing in intact and chemodenervated awake dogs. J Appl Physiol 35: 35-41, 1978.
5. Bernard DG, Li A, and Nattie EE. Evidence for central chemoreception in the midline raphé. J Appl Physiol 80: 108-115, 1996.
6. Bianchi AL, Denavit-Saubié M, and Champagnat J. Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol Rev 75: 1-45, 1995.
7. Bisgard GE and Forster HV. Ventilatory responses to acute and chronic hypoxia. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 4, vol. II, chapt. 52, p. 1207-1239.
8. Bisgard GE, Forster HV, and Klein JP. Recovery of peripheral chemoreceptor function after denervation in ponies. J Appl Physiol 49: 964-970, 1980.
9. Bisgard GE, Forster HV, Orr JA, Buss DD, Rawlings CA, and Rasmussen B. Hypoventilation in ponies after carotid body denervation. J Appl Physiol 40: 184-190, 1976.
10. Bouverot P, Candas V, and Libert JP. Role of the arterial chemoreceptors in ventilatory adaptation to hypoxia of awake dogs and rabbits. Respir Physiol 17: 209-219, 1973.
11. Breslav IS and Konza EA. Restoration of the chemoreceptor function after deafferentation of the sino-carotid zones in rats. Sechenov Physiol J USSR 61: 84-89, 1975.
12. Brice AG, Forster HV, Pan LG, Lowry TF, Murphy CL, and Mend J. Effects of increased end-expiratory lung volume on breathing of awake ponies. J Appl Physiol 70: 715-725, 1991.
13. Brice AG, Forster HV, Pan LG, Funahashi A, Hoffman MD, Murphy CL, and Lowry TF. Is the hyperpnea of muscular contractions critically dependent on spinal afferents? J Appl Physiol 64: 226-233, 1988.
14. Busch MA, Bisgard GE, and Forster HV. Ventilatory acclimatization to hypoxia is not dependent on arterial hypoxemia. J Appl Physiol 58: 1874-1880, 1985.
15. Clifford PS, Coon RL, Von Colditz JH, Zuperku EJ, and Kampine JP. Pulmonary denervation in the dog. J Appl Physiol 54: 1451-1456, 1983.
16. Coates EL, Li A, and Nattie EE. Widespread sites of brain stem ventilatory chemoreceptors. J Appl Physiol 75: 5-14, 1993.
17. Comroe JH Jr and Schmidt CF. The part played by reflexes from the carotid body in the chemical regulation of respiration in the dog. Am J Physiol 121: 75-97, 1938.
18. Davenport HW, Brewer G, Chambers AH, and Goldschmidt S. The respiratory responses to anoxemia of unanesthetized dogs with chronically denervated aortic and carotid chemoreceptors and their causes. Am J Physiol 148: 406-416, 1947.
19. 2 decreases membrane conductance and depolarizes neurons in the nucleus tractus solitarii. Exp Brain Res 76: 656-661, 1989.
20. Duron B. Intercostal and diaphragmatic muscle endings and afferents. In: Regulation of Breathing: Lung Biology in Health and Disease, edited by Hornbein TF. New York: Dekker, 1981, vol. 17, chapt. 7, p. 473-540.
21. Edmunds LH, Graf PD, and Nadel JA. Reinnervation of the reimplanted canine lung. J Appl Physiol 31: 722-727, 1971.
22. Erickson BK, Forster HV, Lowry TF, Pan LG, Korducki MJ, Forster AL, and Forster MA. Changes in respiratory muscle activity in ponies when end-expiratory lung volume is increased. J Appl Physiol 76: 2015-2025, 1994.
23. Feldman JL and Smith JC. Neural control of respiratory pattern in mammals: an overview. In: Regulation of Breathing (2nd ed.), edited by Dempsey JA and Pack AI. New York: Dekker, 1997, vol. 79, p. 39-70. (Lung Biol. Health Dis. Ser.)
24. Flynn C, Forster HV, Pan LG, and Bisgard GE. Role of the hilar nerve afferents in the hyperpnea of exercise. J Appl Physiol 59: 798-806, 1985.
25. Forster HV, Bisgard GE, and Klein JP. Effect of peripheral chemoreceptor denervation on acclimatization of goats during hypoxia. J Appl Physiol 50: 392-398, 1981.
26. Forster HV, Bisgard GE, Rasmussen B, Orr JA, Buss DD, and Manohar M. Ventilatory control in peripheral chemoreceptor-denervated ponies during chronic hypoxemia. J Appl Physiol 41: 878-885, 1976.
27. 2 of humans during submaximal exercise. J Appl Physiol 75: 1385-1394, 1993.
28. Forster HV, Lowry TF, Pan LG, Erickson BK, Korducki MJ, and Forster MA. Diaphragm and lung afferents contribute to inspiratory load compensation in awake ponies. J Appl Physiol 76: 1330-1339, 1994.
29. Forster HV, Ohtake PJ, Pan LG, and Lowry TF. Effect on breathing of surface ventrolateral medullary cooling in awake, anesthetized and asleep goats. Respir Physiol 110: 187-198, 1997.
30. Forster HV, Pan LG, Flynn C, and Bisgard GE. Attentuated Hering-Breuer inflation reflex 4 years after pulmonary vagal denervation in ponies. J Appl Physiol 69: 2163-2167, 1990.
31. Forster HV, Pan LG, Lowry TF, Serra A, Wenninger J, and Martino P. Important role of carotid chemoreceptor afferents in control of breathing of adult and neonatal mammals. Respir Physiol 119: 199-208, 2000.
32. Fuller DD, Johnson SM, Johnson RA, and Mitchell GS. Chronic cervical spinal sensory denervation reveals ineffective spinal pathways to phrenic motoneurons in the rat. Neurosci Lett 323: 25-28, 2002.
33. Gautier H and Bertrand F. Respiratory effects of pneumotoxic center lesions and subsequent vagotomy in chronic cats. Respir Physiol 23: 71-85, 1975.
34. Gautier H and Bonora M. Effects of carotid body denervation on respiratory pattern of awake cats. J Appl Physiol 46: 1127-1131, 1979.
35. Golder FJ, Reier PJ, and Bolser DC. Altered respiratory motor drive after spinal cord injury: supraspinal and bilateral effects of a unilateral lesion. J Neurol 21: 8680-8689, 2001.
36. Goshgarian HG. Developmental plasticity in the respiratory pathway of the adult rat. Exp Neurol 66: 547-555, 1979.
37. Goshgarian HG. The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomena. Exp Neurol 72: 211- 225, 1981.
38. Goshgarian HG, Ellenberger HH, and Feldman JL. Bulbosinal respiratory neurons are a source of double synapses onto phrenic motoneurons following cervical spinal cord hemisection in adult rats. Brain Res 600: 169-173, 1993.
39. Gray PA, Janczewski WA, Mellen N, McCrimmon DR, and Jack Feldman L. Normal breathing requires pre-Bötzinger complex neurokinin-1 receptor-expressing neurons. Nature Neurosci 4: 927-930, 2001.
40. Hadley SD, Walker PD, and Goshgarian HG. Effects of serotonin inhibition on neuronal and astrocyte plasticity in the phrenic nucleus 4 h following C2 spinal cord hemisection. Exp Neurol 160: 433-445, 1999.
41. Hadley SD, Walker PD, and Goshgarian HG. Effects of the serotonin synthesis inhibitor p-CPA on the expression of the crossed phrenic phenomenon 4 h following C2 spinal cord hemisection. Exp Neurol 160: 479-488, 1999.
42. Honda Y, Myojo S, Hasegawa S, Hawegawa T, and Severinghaus JW. Decreased exercise hyperpnea in patients with bilateral carotid chemoreceptor resection. J Appl Physiol 46: 908-912, 1979.
43. Honda Y, Watanabe S, Hashizume I, Satomura Y, Hata N, Sakakibara Y, and Severinghaus JW. Hypoxic chemosensitivity in asthmatic patients two decades after carotid body resection. J Appl Physiol 46: 632-638, 1979.
44. Iber C, Simon P, Skatrud JB, Mahowald MW, and Dempsey JA. The Breuer-Hering reflex in humans: effects of pulmonary denervation and hypocapnia. Am J Respir Crit Care Med 152: 217-224, 1995.
45. Jammes Y and Speck DF. Respiratory control by diaphragmatic and respiratory muscle afferents. In: Regulation of Breathing: Lung Biology in Health and Disease (2nd ed.), edited by Dempsey JA and Pack AI. New York: Dekker, 1995, vol. 79, p. 543-582.
46. Jenkins WM, Merzenick MM, Ocho MT, Allard T, GurcRobles WE. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behavioral controlled tactile stimulation. J Neurophysiol 63: 83-104, 1990.
47. Johnson RA, Okragly AJ, Haak-Frendscho M, and Mitchell GS. Cervical dorsal rhizotomy increases brain-derived neurotrophic factor and neurotrophin-3 expression in the ventral spinal cord. J Neurosci 20: RC77 (1-5), 2000.
48. Johnson SM, Trouth CO, and Smith JC. Chemosensitivity of respiratory pacemaker neurons in the pre-Bötzinger complex in vitro. Soc Neurosci Abstr 24: 346.7, 1998.
49. Kandel ER, Schwartz JH, and Jessell TM. Principles of Neural Science (4th ed.). New York: McGraw-Hill, 2000.
50. Kao FF. An experimental study of pathways invoked in exercise hyperpnea employing cross circulation techniques. In: The Regulation of Human Respiration, edited by Cunningham DJC and Lloyd BB. Oxford, UK: Blackwell, 1963, p. 461-502.
51. Kinkead R, Bach KB, Johnson SM, Hodgeman BA, and Mitchell GS. Plasticity in respiratory motor control: intermittent hypoxia and hypercapnia activate opposing serotonergic and noradrenergic modulatory systems. Comp Biochem Physiol A 130: 207-218, 2001.
52. Kinkead R, Zhan WZ, Prakosh YS, Bach KB, Sieck GS, and Mitchell GS. Cervical dorsal rhizotomy enhances innervation of phrenic motoneurons and serotonin-dependent longterm facilitation of respiratory motor output in rats. J Neurosci 18: 8436-8443, 1998.
53. Ling L, Bach KB, and Mitchell GS. Serotonin reveals ineffective spinal pathways to contralateral phrenic motoneurons in spinally hemisected rats. Exp Brain Res 101: 35-43, 1994.
54. Ling L, Olson EB Jr, Vidruk EH, and Mitchell GS. Attenuation of the hypoxic ventilatory response in adult rats following one month of perinatal hyperoxia. J Physiol 495: 561-571, 1996.
55. Ling L, Olson EB Jr, Vidruk EH, and Mitchell GS. Developmental plasticity of the hypoxic ventilatory response. Respir Physiol 110: 261-268, 1997.
56. Lowry TF, Forster HV, Pan LG, Korducki MA, Probst J, Franciosi RA, and Forster MM. The effect on breathing of carotid body, denervation in neonatal goats. J Appl Physiol 87: 1026-1034, 1999.
57. Lowry TL, Forster HV, Pan LG, Serra A, Wenninger J, Nash R, Sheridan D, and Franciosi RA. Effects on breathing of carotid body denervation in neonatal piglets. J Appl Physiol 87: 2128-2135, 1999.
58. Lugliani R, Whipp BJ, Seard C, and Wasserman K. Effect of bilateral carotid-body resection on ventilatory control at rest and during exercise in man. N Engl J Med 285: 1105-1111, 1971.
59. Lumsden T. Observations on the respiratory centers in the cat. J Physiol 57: 153-160, 1928.
60. Martin-Body RL, Robson GJ, and Sinclair JD. Restoration of hypoxic responses in the awake rat after carotid body denervation by sinus nerve section. J Physiol 380: 61-73, 1986.
61. Mathew OP and Ghosh TK. Role of airway afferents on upper airway muscle activity. In: Regulation of Breathing: Lung Biology in Health and Disease (2nd ed.), edited by Dempsey JA and Pack AI. New York: Dekker, 1995, vol. 79, p. 511-542.
62. Mazza E, Edelman NH, and Neubauer JA. Hypoxic excitation in neurons cultured from the rostral ventrolateral medulla of the neonatal rat. J Appl Physiol 88: 2319-2329, 2000.
63. Mitchell GS, Bach KB, Martin PA, Foley KT, Olson EB, Brownfield MS, Miletic V, Behan M, McGuirk S, and Sloan HE. Increased spinal monoamine concentrations after chronic thoracic dorsal rhizotomy in goats. J Appl Physiol 89: 1266-1274, 2000.
64. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, and Olson EB Jr. Invited Review: Intermittent hypoxia and respiratory plasticity. J Appl Physiol 90: 2466-2475, 2001.
65. Mitchell GS, Douse MA, and Foley KT. Receptor interactions in modulating ventilatory activity. Am J Physiol Regul Integr Comp Physiol 259: R911-R920, 1990.
66. Mitchell GS and Johnson SM. Invited Review: Neuroplasticity in respiratory motor control. J Appl Physiol 94: 358-374, 2003.
67. Morrell MJ, Heywood P, Moosavi SH, Guz A, and Stevens J. Unilateral focal lesions in the rostrolateral medulla influence chemosensitivity and breathing measured during wakefulness, sleep, and exercise. J Neurol Neurosurg Psychiatry 67: 637-645, 1999.
68. Nattie EE. Central chemoreceptors. In: Regulation of Breathing (2nd ed.), edited by Dempsey JA and Pack AI. New York: Dekker, 1997, vol. 79, p. 473-510. (Lung Biol. Health Dis. Ser.)
69. Nattie EE and Li A. Fluorescence location of RVLM kainate microinjections that alter the control of breathing. J Appl Physiol 68: 1157-1166, 1990.
70. Nattie EE, Li A, and St John WM. Lesions in retrotrapezoid nucleus decrease ventilatory output in anesthetized or decerebrate cats. J Appl Physiol 71: 1364-1375, 1991.
71. Nielsen AM, Bisgard GE, and Vidruk EH. Carotid chemoreceptor activity during acute and sustained hypoxia in goats. J Appl Physiol 65: 1796-1802, 1988.
72. O'Hara TE and Goshgarian HG. Quantitative assessment of phrenic nerve functional recovery mediated by the crossed phrenic reflex at various time intervals after spinal cord injury. Exp Neurol 111: 244-250, 1991.
73. Onimaru H and Homma I. Respiratory rhythm generator in the medulla of brain stem-spinal cord preparation from newborn rat. Brain Res 403: 380-384, 1987.
74. Pan LG, Forster HV, Bisgard GE, Kaminski RP, Dorsey SM, and Busch MA. Hyperventilation in ponies at the onset of and during steady-state exercise. J Appl Physiol 54: 1394-1402, 1983.
75. Pan LG, Forster HV, Martino P, Strecker PJ, Beales J, Serra A, Lowry TF, Forster MM, and Forster AL. Important role of carotid afferents in control of breathing. J Appl Physiol 85: 1299-1306, 1998.
76. Pan LG, Forster HV, Wurster RD, Murphy CL, Brice AG, and Lowry TF. Effect of partial spinal cord ablation on exercise hyperpnea in ponies. J Appl Physiol 69: 1821-1827, 1990.
77. Pan LG, Forster HV, Wurster RD, Brice AG, and Lowry TF. Effect of multiple denervations on the exercise hyperpnea in awake ponies. J Appl Physiol 79: 302-311, 1995.
78. Petrozzino JJ, Scardella AT, Santiago TV, and Edelman NH. Dichloroacetate blocks endogenous opioid effects during inspiratory flow-resistive loading. J Appl Physiol 72: 590-596, 1992.
79. Porter WT. The path of the respiratory impulse from the bulb to the phrenic nuclei. J Physiol 17: 455-485, 1895.
80. Rodman JR, Curran AK, Henderson KS, Dempsey JA, and Smith CA. Carotid body denervation in dogs: eupnea and the ventilatory response to hyperoxic hypercapnia. J Appl Physiol 91: 328-335, 2001.
81. Secrist WL and Trummer MJ. Nerve regeneration following lung reimplantation. Ann Thorac Surg 4: 125-132, 1967.
82. Serra A, Brozoski D, Hedin N, Franciosi RA, and Forster HV. Mortality after carotid body denervation in rats. J Appl Physiol 91: 1298-1306, 2001.
83. Serra A, Brozoski D, Hodges M, Roethle S, Franciosi R, and Forster HV. Effects of carotid and aortic chemoreceptor denervation in newborn piglets. J Appl Physiol 92: 893-900, 2002.
84. Serra A, Brozoski D, Simeon T, Yi J, Bastasic J, Franciosi R, Jacobs ER, and Forster HV. Serotonin and serotonin receptor expression in the aorta of carotid intact or denervated newborns. Respir Physiol 132: 253-264, 2002.
85. Shea SA, Horner RL, Banner NR, McKenzie E, Heaton R, Yacoub MH, and Guz A. The effect of human heart-lung transplantation upon breathing at rest and during sleep. Respir Physiol 72: 131-149, 1988.
86. Smith CA, Saupe KW, Henderson KS, and Dempsey JA. Ventilatory effects of specific carotid body hypocapnia in the dog during wakefulness and sleep. J Appl Physiol 79: 689-699, 1995.
87. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, and Feldman JL. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
88. Smith PG and Mills E. Restoration of reflex ventilatory response to hypoxia after removal of carotid bodies in the cat. Neuroscience 4: 573-580, 1980.
89. Solomon IC, Edelman NH, and Neubauer JA. Pre-Bötzinger complex function as a central hypoxic chemosensor for respiration in vivo. J Neurophysiol 83: 2854-2868, 2000.
90. Speck DF. Bötzinger complex role in phrenic-to-phrenic inhibitory reflex of cat. J Appl Physiol 67: 1364-1370, 1989.
91. St. John WM. Medullary regions for neurogenesis of gasping: noeud vital or noeuds vitals? J Appl Physiol 81: 1865-1877, 1996.
92. St. John WM. Respiratory tidal volume responses of cats with chronic pneumotaxic center lesions. Respir Physiol 16: 92-108, 1972.
93. St. John WM, Glasser RL, and King RA. Rhythmic respiration in awake vagotomized cats with chronic pneumotaxic area lesions. Respir Physiol 15: 233-244, 1972.
94. Teitelbaum JS, Magder SA, Roussos C, and Hussain SNA. Effects of diaphragmatic ischemia on the inspiratory motor drive. J Appl Physiol 72: 447-454, 1992.
95. Wade JG, Larsohn CP Jr, Hickey RF, Ehrenfeld WK, and Severinghaus JW. Effect of carotid endarterectomy on carotid chemoreceptor and baroreceptor function in man. N Engl J Med 282: 823-829, 1970.
96. Wasserman K, Whipp BJ, Koyal SN, and Cleary MG. Effect of carotid body resection on ventilatory and acid-base control during exercise. J Appl Physiol 39: 354-358, 1975.
97. Watt JG, Dumke PR, and Comroe JH. Effects of inhalation of 100 percent and 14 percent oxygen upon respiration of unanesthetized dogs before and after chemoreceptor denervation. Am J Physiol 138: 610-617, 1942.
98. Wenninger JM, Pan LG, Martino P, Geiger L, Hodges M, Serra A, Feroah TR, and Forster HV. Multiple rostral medullary nuclei can influence breathing in awake goats. J Appl Physiol 91: 777-788, 2001.
99. Widdicombe JG. Nervous receptors in the respiratory tract and lungs. In: Regulation of Breathing: Lung Biology in Health and Disease, edited by Hornbein TF. New York: Dekker, 1981, vol. 17, chapt. 6, p. 429-472.
100. Zhou S and Goshgarian HG. 5-Hydroxytryptophan-induced respiratory recovery after cervical spinal cord hemisection in rats. J Appl Physiol 89: 1428-1536, 2000.